Testing the local mate competition rule in a quasi-gregarious parasitoid with facultative superparasitism

As an important domain of evolutionary ecology, sex allocation theory well explains the evolution of investment into female versus male offspring. Local mate competition (LMC) is a good predictor of sex allocation, where the optimal sex ratio becomes less female-biased and asymptotically approaches 0.5 as the number of foundresses increases. Parasitoid wasps, with haplodiploid sex determination, offer excellent opportunities to test how organisms manipulate their offspring sex ratio in response to environmental variation, and many species have been proven to allocate sex according to predictions under LMC. When hosts are spatially clustered, as in gregarious species, the mating systems of quasi-gregarious parasitoids meet the essential assumptions (female mating before dispersal) of LMC. However, inconsistent with predictions, in the quasi-gregarious species Anastatus disparis (Hymenoptera: Eupelmidae), a strongly female-biased eclosion sex ratio (0.156±0.018 to 0.185±0.016) was observed as the number of females laying eggs in a patch increased. Superparasitism, in which 44.7% of parasitized hosts contained more than one egg but only one adult emerged from each host, was common in A. disparis. However, the egg sex ratio was determined by microsatellites and likely fit the predictions of LMC theory. Male-biased offspring mortality arising from superparasitism during development likely contributes to the shift from the primary sex ratio predicted under LMC to the observed female-biased eclosion sex ratio. Inconsistent with results in gregarious parasitoids, the role of superparasitism in driving sex ratio shifts in quasi-gregarious parasitoids should be incorporated into LMC-based predictions of sex ratios.

作为进化生态学的重要研究领域，性分配理论可较好阐释雌性与雄性后代的资源投入演化规律。局部配偶竞争（Local Mate Competition, LMC）是性分配模式的有效预测因子：随着单块寄主斑块内产卵雌蜂数量增加，最优性比的雌性偏向程度逐渐降低，最终渐近趋近于0.5。具有单倍二倍体性别决定机制的寄生蜂，为探究生物体如何响应环境变化调控子代性比提供了理想的实验模型，且已有诸多物种被证实能够依据LMC理论的预测进行性分配。当寄主呈空间聚集分布时（如群栖性物种），准群栖性寄生蜂的交配系统符合LMC的核心假设——雌蜂在扩散前完成交配。然而，与理论预测相悖的是，在准群栖性物种舞毒蛾黑卵蜂（Anastatus disparis，膜翅目：旋小蜂科）中，随着单块寄主斑块内产卵雌蜂数量增加，观测到的羽化性比呈现强烈的雌性偏向（0.156±0.018 至 0.185±0.016）。超寄生现象在舞毒蛾黑卵蜂中极为普遍：44.7%的被寄生寄主含有多枚蜂卵，但每个寄主仅能羽化出1头成虫。不过，通过微卫星标记分析得到的卵期性比，却符合LMC理论的预测结果。发育阶段因超寄生引发的雄性子代死亡，可能是导致从LMC预测的初级性比偏移至观测到的雌性偏向羽化性比的核心诱因。与群栖性寄生蜂的研究结论相悖，准群栖性寄生蜂中超寄生对性比偏移的调控作用，应当被纳入基于LMC的性比预测模型中。